. 2021 Jul 6;16(1):301.

doi: 10.1186/s13023-021-01917-y.

Rare manifestations and malignancies in tuberous sclerosis complex: findings from the TuberOus SClerosis registry to increAse disease awareness (TOSCA)

Matthias Sauter¹, Elena Belousova², Mirjana P Benedik³, Tom Carter⁴, Vincent Cottin⁵, Paolo Curatolo⁶, Maria Dahlin⁷, Lisa D'Amato⁸, Guillaume B d'Augères⁹, Petrus J de Vries¹⁰, José C Ferreira¹¹, Martha Feucht¹², Carla Fladrowski^{13

14}, Christoph Hertzberg¹⁵, Sergiusz Jozwiak^{16

17}, John A Lawson¹⁸, Alfons Macaya¹⁹, Ruben Marques^{8

20}, Rima Nabbout²¹, Finbar O'Callaghan²², Jiong Qin²³, Valentin Sander²⁴, Seema Shah²⁵, Yukitoshi Takahashi²⁶, Renaud Touraine²⁷, Sotiris Youroukos²⁸, Bernard Zonnenberg²⁹, Anna Jansen³⁰, J Chris Kingswood³¹; TOSCA investigators

Collaborators, Affiliations

Collaborators

TOSCA investigators:
Nobuo Shinohara, Shigeo Horie, Masaya Kubota, Jun Tohyama, Katsumi Imai, Mari Kaneda, Hideo Kaneko, Yasushi Uchida, Tomoko Kirino, Shoichi Endo, Yoshikazu Inoue, Katsuhisa Uruno, Ayse Serdaroglu, Zuhal Yapici, Banu Anlar, Sakir Altunbasak, Olga Lvova, Oleg Valeryevich Belyaev, Oleg Agranovich, Elena Vladislavovna Levitina, Yulia Vladimirovna Maksimova, Antonina Karas, Yuwu Jiang, Liping Zou, Kaifeng Xu, Yushi Zhang, Guoming Luan, Yuqin Zhang, Yi Wang, Meiling Jin, Dingwei Ye, Weiping Liao, Liemin Zhou, Jie Liu, Jianxiang Liao, Bo Yan, Yanchun Deng, Li Jiang, Zhisheng Liu, Shaoping Huang, Hua Li, Kijoong Kim, Pei-Lung Chen, Hsiu-Fen Lee, Jeng-Dau Tsai, Ching-Shiang Chi, Chao-Ching Huang, Kate Riney, Deborah Yates, Patrick Kwan, Surachai Likasitwattanakul, Charcrin Nabangchang, Lunliya Thampratankul Krisnachai Chomtho, Kamornwan Katanyuwong, Somjit Sriudomkajorn, Jo Wilmshurst, Reeval Segel, Tal Gilboa, Michal Tzadok, Aviva Fattal- Valevski, Panagiotis Papathanasopoulos, Antigone Syrigou Papavasiliou, Stylianos Giannakodimos, Stylianos Gatzonis, Evangelos Pavlou, Meropi Tzoufi, A M H Vergeer, Marc Dhooghe, Hélène Verhelst, Filip Roelens, Marie Cecile Nassogne, Pierre Defresne, Liesbeth De Waele, Patricia Leroy, Nathalie Demonceau, Benjamin Legros, Patrick Van Bogaert, Berten Ceulemans, Lina Dom, Pierre Castelnau, Anne De Saint Martin, Audrey Riquet, Mathieu Milh, Claude Cances, Jean-Michel Pedespan, Dorothee Ville, Agathe Roubertie, Stéphane Auvin, Patrick Berquin, Christian Richelme, Catherine Allaire, Sophie Gueden, Sylvie Nguyen The Tich, Bertrand Godet, Maria Luz Ruiz Falco Rojas, Jaume Campistol Planas, Antonio Martinez Bermejo, Patricia Smeyers Dura, Susana Roldan Aparicio, Maria Jesus Martinez Gonzalez, Javier Lopez Pison, Manuel Oscar Blanco Barca, Eduardo Lopez Laso, Olga Alonso Luengo, Francisco Javier Aguirre Rodriguez, Ignacio Malaga Dieguez, Ana Camacho Salas, Itxaso Marti Carrera, Eduardo Martinez Salcedo, Maria Eugenia Yoldi Petri, Ramon Cancho Candela, Ines da Conceicao Carrilho, Jose Pedro Vieira, José Paulo da Silva Oliveira Monteiro, Miguel Jorge Santos de Oliveira Ferreira Leao, Catarina Sofia Marceano Ribeiro Luis, Carla Pires Mendonca, Milda Endziniene, Jurgis Strautmanis, Inga Talvik, Maria Paola Canevini, Antonio Gambardella, Dario Pruna, Salvatore Buono, Elena Fontana, Bernardo Dalla Bernardina, Carmen Burloiu, Iuliu Stefan Bacos Cosma, Mihaela Adela Vintan, Laura Popescu, Karel Zitterbart, Jaroslava Payerova, Ladislav Bratsky, Zuzana Zilinska, Ursula Gruber-Sedlmayr, Matthias Baumann, Edda Haberlandt, Kevin Rostasy, Ekaterina Pataraia, Frances Elmslie, Clare Ann Johnston, Pamela Crawford, Peter Uldall, Paul Uvebrant, Olof Rask, Marit Bjoernvold, Eylert Brodtkorb, Andreas Sloerdahl, Ragnar Solhoff, Martine Sofie Gilje Jaatun, Marek Mandera, Elzbieta Janina Radzikowska, Mariusz Wysocki, Michael Fischereder, Gerhard Kurlemann, Bernd Wilken, Adelheid Wiemer-Kruel, Klemens Budde, Klaus Marquard, Markus Knuf, Andreas Hahn, Hans Hartmann, Andreas Merkenschlager, Regina Trollmann

Affiliations

¹ Klinikum Kempten, Klinikverbund Allgäu, Robert-Weixler-Str. 50, 87439, Kempten, Germany. Matthias.Sauter@klinikverbund-allgaeu.de.
² Research and Clinical Institute of Pediatrics, Pirogov Russian National Research Medical University, Moscow, Russian Federation.
³ SPS Pediatrična Klinika, Ljubljana, Slovenia.
⁴ TSA Tuberous Sclerosis Association, Nottingham, UK.
⁵ Hôpital Louis Pradel, Claude Bernard University Lyon 1, Lyon, France.
⁶ Tor Vergata University Hospital, Rome, Italy.
⁷ Karolinska University Hospital, Stockholm, Sweden.
⁸ Novartis Farma S.P.A, Origgio, Italy.
⁹ Association Sclérose Tubéreuse de Bourneville, Gradignan, France.
¹⁰ Division of Child and Adolescent Psychiatry, University of Cape Town, Cape Town, South Africa.
¹¹ Centro Hospitalar Lisboa Ocidental, Lisbon, Portugal.
¹² Universitätsklinik Für Kinder-Und Jugendheilkunde (Affiliated Partner of the ERN EpiCARE), Vienna, Austria.
¹³ Associazione Sclerosi Tuberosa ONLUS, Milan, Italy.
¹⁴ In Den Birken, European Tuberous Sclerosis Complex Association, Dattein, Germany.
¹⁵ Vivantes-Klinikum Neukölln, Berlin, Germany.
¹⁶ Department of Child Neurology, Medical University of Warsaw, Warsaw, Poland.
¹⁷ Department of Neurology and Epileptology, The Children's Memorial Health Institute, Warsaw, Poland.
¹⁸ The Tuberous Sclerosis Multidisciplinary Management Clinic, Sydney Children's Hospital, Randwick, NSW, Australia.
¹⁹ Hospital Universitari Vall D'Hebron, Barcelona, Spain.
²⁰ Institute of Biomedicine (IBIOMED), University of León, León, Spain.
²¹ Department of Pediatric Neurology, Necker Enfants Malades Hospital, Imagine Institute, Paris Descartes University, Paris, France.
²² Institute of Child Health, University College London, London, UK.
²³ Department of Pediatrics, Peking University People's Hospital, Beijing, China.
²⁴ Tallinn Children Hospital, Tallinn, Estonia.
²⁵ Novartis Healthcare Pvt. Ltd, Hyderabad, India.
²⁶ National Epilepsy Center, Shizuoka Institute of Epilepsy and Neurological Disorders, Aoi-ku, UrushiyamaShizuoka, Japan.
²⁷ Department of Genetics, CHU-Hôpital Nord, Saint Etienne, France.
²⁸ St. Sophia Children's Hospital, Athens, Greece.
²⁹ University Medical Center, Utrecht, The Netherlands.
³⁰ Pediatric Neurology Unit, Department of Pediatrics, UZ Brussel VUB, Brussels, Belgium.
³¹ Cardiology Clinical Academic Group, Molecular and Clinical Sciences Research Centre, St Georges University of London, London, UK.

PMID: 34229737
PMCID: PMC8259106
DOI: 10.1186/s13023-021-01917-y

Rare manifestations and malignancies in tuberous sclerosis complex: findings from the TuberOus SClerosis registry to increAse disease awareness (TOSCA)

Matthias Sauter et al. Orphanet J Rare Dis. 2021.

. 2021 Jul 6;16(1):301.

doi: 10.1186/s13023-021-01917-y.

Authors

Collaborators

TOSCA investigators:
Nobuo Shinohara, Shigeo Horie, Masaya Kubota, Jun Tohyama, Katsumi Imai, Mari Kaneda, Hideo Kaneko, Yasushi Uchida, Tomoko Kirino, Shoichi Endo, Yoshikazu Inoue, Katsuhisa Uruno, Ayse Serdaroglu, Zuhal Yapici, Banu Anlar, Sakir Altunbasak, Olga Lvova, Oleg Valeryevich Belyaev, Oleg Agranovich, Elena Vladislavovna Levitina, Yulia Vladimirovna Maksimova, Antonina Karas, Yuwu Jiang, Liping Zou, Kaifeng Xu, Yushi Zhang, Guoming Luan, Yuqin Zhang, Yi Wang, Meiling Jin, Dingwei Ye, Weiping Liao, Liemin Zhou, Jie Liu, Jianxiang Liao, Bo Yan, Yanchun Deng, Li Jiang, Zhisheng Liu, Shaoping Huang, Hua Li, Kijoong Kim, Pei-Lung Chen, Hsiu-Fen Lee, Jeng-Dau Tsai, Ching-Shiang Chi, Chao-Ching Huang, Kate Riney, Deborah Yates, Patrick Kwan, Surachai Likasitwattanakul, Charcrin Nabangchang, Lunliya Thampratankul Krisnachai Chomtho, Kamornwan Katanyuwong, Somjit Sriudomkajorn, Jo Wilmshurst, Reeval Segel, Tal Gilboa, Michal Tzadok, Aviva Fattal- Valevski, Panagiotis Papathanasopoulos, Antigone Syrigou Papavasiliou, Stylianos Giannakodimos, Stylianos Gatzonis, Evangelos Pavlou, Meropi Tzoufi, A M H Vergeer, Marc Dhooghe, Hélène Verhelst, Filip Roelens, Marie Cecile Nassogne, Pierre Defresne, Liesbeth De Waele, Patricia Leroy, Nathalie Demonceau, Benjamin Legros, Patrick Van Bogaert, Berten Ceulemans, Lina Dom, Pierre Castelnau, Anne De Saint Martin, Audrey Riquet, Mathieu Milh, Claude Cances, Jean-Michel Pedespan, Dorothee Ville, Agathe Roubertie, Stéphane Auvin, Patrick Berquin, Christian Richelme, Catherine Allaire, Sophie Gueden, Sylvie Nguyen The Tich, Bertrand Godet, Maria Luz Ruiz Falco Rojas, Jaume Campistol Planas, Antonio Martinez Bermejo, Patricia Smeyers Dura, Susana Roldan Aparicio, Maria Jesus Martinez Gonzalez, Javier Lopez Pison, Manuel Oscar Blanco Barca, Eduardo Lopez Laso, Olga Alonso Luengo, Francisco Javier Aguirre Rodriguez, Ignacio Malaga Dieguez, Ana Camacho Salas, Itxaso Marti Carrera, Eduardo Martinez Salcedo, Maria Eugenia Yoldi Petri, Ramon Cancho Candela, Ines da Conceicao Carrilho, Jose Pedro Vieira, José Paulo da Silva Oliveira Monteiro, Miguel Jorge Santos de Oliveira Ferreira Leao, Catarina Sofia Marceano Ribeiro Luis, Carla Pires Mendonca, Milda Endziniene, Jurgis Strautmanis, Inga Talvik, Maria Paola Canevini, Antonio Gambardella, Dario Pruna, Salvatore Buono, Elena Fontana, Bernardo Dalla Bernardina, Carmen Burloiu, Iuliu Stefan Bacos Cosma, Mihaela Adela Vintan, Laura Popescu, Karel Zitterbart, Jaroslava Payerova, Ladislav Bratsky, Zuzana Zilinska, Ursula Gruber-Sedlmayr, Matthias Baumann, Edda Haberlandt, Kevin Rostasy, Ekaterina Pataraia, Frances Elmslie, Clare Ann Johnston, Pamela Crawford, Peter Uldall, Paul Uvebrant, Olof Rask, Marit Bjoernvold, Eylert Brodtkorb, Andreas Sloerdahl, Ragnar Solhoff, Martine Sofie Gilje Jaatun, Marek Mandera, Elzbieta Janina Radzikowska, Mariusz Wysocki, Michael Fischereder, Gerhard Kurlemann, Bernd Wilken, Adelheid Wiemer-Kruel, Klemens Budde, Klaus Marquard, Markus Knuf, Andreas Hahn, Hans Hartmann, Andreas Merkenschlager, Regina Trollmann

Affiliations

¹ Klinikum Kempten, Klinikverbund Allgäu, Robert-Weixler-Str. 50, 87439, Kempten, Germany. Matthias.Sauter@klinikverbund-allgaeu.de.
² Research and Clinical Institute of Pediatrics, Pirogov Russian National Research Medical University, Moscow, Russian Federation.
³ SPS Pediatrična Klinika, Ljubljana, Slovenia.
⁴ TSA Tuberous Sclerosis Association, Nottingham, UK.
⁵ Hôpital Louis Pradel, Claude Bernard University Lyon 1, Lyon, France.
⁶ Tor Vergata University Hospital, Rome, Italy.
⁷ Karolinska University Hospital, Stockholm, Sweden.
⁸ Novartis Farma S.P.A, Origgio, Italy.
⁹ Association Sclérose Tubéreuse de Bourneville, Gradignan, France.
¹⁰ Division of Child and Adolescent Psychiatry, University of Cape Town, Cape Town, South Africa.
¹¹ Centro Hospitalar Lisboa Ocidental, Lisbon, Portugal.
¹² Universitätsklinik Für Kinder-Und Jugendheilkunde (Affiliated Partner of the ERN EpiCARE), Vienna, Austria.
¹³ Associazione Sclerosi Tuberosa ONLUS, Milan, Italy.
¹⁴ In Den Birken, European Tuberous Sclerosis Complex Association, Dattein, Germany.
¹⁵ Vivantes-Klinikum Neukölln, Berlin, Germany.
¹⁶ Department of Child Neurology, Medical University of Warsaw, Warsaw, Poland.
¹⁷ Department of Neurology and Epileptology, The Children's Memorial Health Institute, Warsaw, Poland.
¹⁸ The Tuberous Sclerosis Multidisciplinary Management Clinic, Sydney Children's Hospital, Randwick, NSW, Australia.
¹⁹ Hospital Universitari Vall D'Hebron, Barcelona, Spain.
²⁰ Institute of Biomedicine (IBIOMED), University of León, León, Spain.
²¹ Department of Pediatric Neurology, Necker Enfants Malades Hospital, Imagine Institute, Paris Descartes University, Paris, France.
²² Institute of Child Health, University College London, London, UK.
²³ Department of Pediatrics, Peking University People's Hospital, Beijing, China.
²⁴ Tallinn Children Hospital, Tallinn, Estonia.
²⁵ Novartis Healthcare Pvt. Ltd, Hyderabad, India.
²⁶ National Epilepsy Center, Shizuoka Institute of Epilepsy and Neurological Disorders, Aoi-ku, UrushiyamaShizuoka, Japan.
²⁷ Department of Genetics, CHU-Hôpital Nord, Saint Etienne, France.
²⁸ St. Sophia Children's Hospital, Athens, Greece.
²⁹ University Medical Center, Utrecht, The Netherlands.
³⁰ Pediatric Neurology Unit, Department of Pediatrics, UZ Brussel VUB, Brussels, Belgium.
³¹ Cardiology Clinical Academic Group, Molecular and Clinical Sciences Research Centre, St Georges University of London, London, UK.

PMID: 34229737
PMCID: PMC8259106
DOI: 10.1186/s13023-021-01917-y

Abstract

Background: Tuberous sclerosis complex (TSC) is a rare multisystem autosomal dominant disorder caused by pathogenic variants in either the TSC1 or TSC2 gene. Common manifestations of TSC have been grouped into major and minor clinical diagnostic criteria and assessed in clinical routine workup. However, case studies point towards the existence of rare disease manifestations and to the potential association of TSC with malignant tumors. In this study we sought to characterize rare manifestations and malignancies using a large cohort of patients.

Methods: TuberOus SClerosis registry to increAse disease awareness (TOSCA) is a multicenter, international disease registry collecting clinical manifestations and characteristics of patients with TSC, both retrospectively and prospectively. We report rates and characteristics of rare manifestations and malignancies in patients with TSC who had enrolled in the TOSCA registry. We also examined these manifestations by age, sex, and genotype (TSC1 or TSC2).

Results: Overall, 2211 patients with TSC were enrolled in the study. Rare manifestations were reported in 382 (17.3%) study participants and malignancies in 65 (2.9%). Of these rare manifestations, the most frequent were bone sclerotic foci (39.5%), scoliosis (23%), thyroid adenoma (5.5%), adrenal angiomyolipoma (4.5%), hemihypertrophy and pancreatic neuroendocrine tumors (pNET; both 3.1%). These rare manifestations were more commonly observed in adults than children (66.2% vs. 22.7%), in females versus males (58.4% vs. 41.6%; except for scoliosis: 48.9% vs. 51.1%), and in those with TSC2 versus TSC1 (67.0% vs. 21.1%; except for thyroid adenoma: 42.9% vs. 57.1%). In the 65 individuals with reported malignancies, the most common were renal cell carcinoma (47.7%), followed by breast (10.8%) and thyroid cancer (9.2%). Although malignancies were more common in adult patients, 26.1% were reported in children and 63.1% in individuals < 40 years. TSC1 mutations were over-represented in individuals with malignancies compared to the overall TOSCA cohort (32.1% vs. 18.5%).

Conclusion: Rare manifestations were observed in a significant proportion of individuals with TSC. We recommend further examination of rare manifestations in TSC. Collectively, malignancies were infrequent findings in our cohort. However, compared to the general population, malignant tumors occurred earlier in age and some tumor types were more common.

Keywords: Malignancy; Rare manifestation; TOSCA; TSC; Tuberous sclerosis complex.

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Conflict of interest statement

MS, EB, TC, VC, PC, GBd’A, JCK, JCF, MF, CF, CH, SJ, RN, FO’C, JQ, RT, MD, JAL, AM, SY, MPB, ACJ, PJdV, and BZ received honoraria and support for travel from Novartis. VC received personal fees for consulting, lecture fees and travel from Actelion, Bayer, Biogen Idec, Boehringer Ingelheim, Gilead, GSK, MSD, Novartis, Pfizer, Roche, Sanofi; grants from Actelion, Boehringer Ingelheim, GSK, Pfizer, Roche; personal fees for developing educational material from Boehringer Ingelheim and Roche. PJdV has been on the study steering group of the EXIST-1, 2 and 3 studies sponsored by Novartis, and co-PI on two investigator-initiated studies part-funded by Novartis. RN received grant support, paid to her institution, from Eisai and lectures fees from Nutricia, Eisai, Advicenne and GW Pharma. YT received personal fees from Novartis for lecture and for copyright of referential figures from the journals and received a grant from the Japanese government for intractable epilepsy research. SJ was partly financed by the EC Seventh Framework Programme (FP7/2007-2013; EPISTOP, grant agreement no. 602391), the Polish Ministerial funds for science (years 2013-2018) for the implementation of international co-financed project and the grant EPIMARKER of the Polish National Center for Research and Development No STRATEGMED3/306306/4/2016. JCK, PC, CH, JAL, and JQ received a research grant from Novartis. RM, LD’A and SS are employees of Novartis. VS and SV reported no conflict of interest. This study was funded by Novartis Pharma AG. All authors approved the final version of the manuscript prior to submission.

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Rare manifestations and malignancies in tuberous sclerosis complex: findings from the TuberOus SClerosis registry to increAse disease awareness (TOSCA)

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Rare manifestations and malignancies in tuberous sclerosis complex: findings from the TuberOus SClerosis registry to increAse disease awareness (TOSCA)

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